Hormonal and histological study on the protective effect of Moringa oleifera against chromium toxicity

Document Type : Research Paper


Department of Biology, College of Science, University of Mosul, Iraq



The current study aimed to know the effects of oral administration of Moringa oleifera leaves powder which contains the active substances to prevent the harmful toxic effect of chromium Cr (potassium dichromate; VI) on some hormonal and biochemical tests, in addition to understand the relationship between active compound of Moringa oleifera on testes and liver tissues against chromium toxicity. Thirty-three healthy male white New Zealand rabbits were randomly distributed in three groups (11 rabbits in each group). The first group were orally drenched normal saline considered as a control group. The second, were treated with chromium (40 mg kg-1 body weight/day) to notice experimental toxicity on some blood parameters and tissues structure., The third with 300 mg Moringa oleifera powder /kg diet/day with the chromium (40 mg kg-1 body weight/day). Treating for all groups was continued for 60 days. The results showed negative effects as a significant decrease (p≤ 0.01) in testosterone and inhibin-B hormone, glutathione (GSH) and total antioxidant capacity (TAC), by the increased level of FSH, alanin amino transferase (ALT), aspartate amino transferase (AST), liver cholesterol and malondialdehyde (MDA), in addition to histological variation in liver and testes in the rabbit serum dealt with chromium (group 2). In contrast, a positive effect was observed as a significant raise in testosterone, inhibin-B hormone, GSH and TAC, by decreased levels of FSH, ALT, AST, liver cholesterol and MDA in the serum dealt with Moringa oleifera (group 3), in addition to the improvement effects on testicular tissue and liver to be closed to normal concentration in control group.


Abdou, H, Bergeron, F & Tremblay, J 2014, A cell-autonomous molecular cascade initiated by amp-activated protein kinase represses steroidogenesis. Molecular and Cellular Biology, 34: 4257-4271.
Abeer, A, Abdel Hameed, M, Attia, T et al.  2018, Protective effects of Moringa oleifera extract on isoniazid and rifampicin induced hepatotoxicity in rats: involvement of adiponectin and tumor necrosis factor-α.
Egyptian Journal of Veterinary Sciences, 49: 25-34.
Acharya, U, Mishra, M, Tripathy, R  et al. 2006, Testicular dysfunction and antioxidative defence system of Swiss mice after chromic acid exposure. Reproductive Toxicology, 22: 87-91.
Achinewu, SC & Aniena, AI 1995, Studies of spices of food value in the south eastern states of Nigeria. Journal of African medicinal plants, 18:135-139.
Afonne, O, Orisakwe, O, Ekanem, I & Akumka, D 2000, Zinc protects chromium-induced testicular injury in mice. Indian Journal of Pharmaceutical Sciences, 34:26-31.
Akunna, G, Ogunmodede, O, Saalu, P & Salawu, E 2012, Ameliorative effect of moringa oleifera (drumstick) leaf extracts on chromium- induced testicular toxicity in rat testes. World Journal of Pharmaceutical and Life Sciences and Medical Research, 2: 20- 27.
Al Hadidy, A & Dawood, S 2021, The effect of moringa oleifera leaves powder on some hormones to prevent the development of experimental hypothyroidism in rabbits. Indian Journal of Forensic Medicine & Toxicology, 15: 1040-1047.
Alizadeh, SM & Mirarab-Razi, J 2016, Growth and accumulation responses of Populus nigra L. exposed to hexavalent chromium excess, Caspian Journal of Environmental Sciences, 14: 253-261.
Al Khafaf, A 2005, Oxidative stress susceptibility to inducing experimental atherosclerotic lesions in female albino rats with the use of some antioxidants. PhD Dissertation, College of Science, University of Mosul, Iraq.
Al Mukhtar, N, Mohmmed, A & Mahdi, H 2016, The effects of potassium dichromate on testes, accessory sex glands, liver and kidney in adult male rats treated with ascorbic acid. Australian Journal of Basic and Applied Sciences. 10: 99-108.
Al Saadi, M & Al kaisei, B 2020, Pathologicl effects of chromium trivalent supplementation in diets of male rabbits exposed to heat stress. Plant Archives, 20: 849-853.
Aybek, H, Aybek, Z, Rota, S, Şen, N & Akbulut, M 2008, The effects of diabetes mellitus, age, and vitamin E on testicular oxidative stress. Fertility & Sterility, 90: 755-760.
Azizi, A, Krika, A, Krika, F 2020, Heavy metal bioaccumulation and distribution in Typha latifolia and Arundo donax: Implication for phytoremediation, Iran. Caspian Journal of Environmental Sciences, 18: 21-29.
Bagchi, D, Stohs, S, Downs, B, Bagchi, M & Preuss, H 2002, Cytotoxicity and oxidative mechanisms of different forms of chromium. Toxicology, 180: 5-22.
Banerjee, S, Joshi, N, Mukherjee, R, Singh, P, Baxi, D & Ramachandran, A 2017, Melatonin protects against chromium (VI) induced hepatic oxidative stress and toxicity: Duration dependent study with realistic dosage. Interdisciplinary Toxicology, 10: 20-29.
Bashandy, S, Ahmed Farid, O, Omara, E, El Toumy, S & Salib, J 2019, Protective effect of citrus reticulata peel extract against potassium dichromate induced reproductive toxicity in rats. Asian Pacific Journal of Reproduction, 8: 267-275.
Bashandy, S, Salama, A, Fayed, A, Omara, E, El Toumy, S & Salib, J 2020, Protective effect of mandarin (citrus reticulata) peel extract on potassium dichromate induced hepatotoxicity and nephrotoxicity in rats. Plant Archives, 20: 2231-2242.
Bedwal, R & Bahuguna, A 1994, Zinc, copper and selenium in reproduction. Experientia, 50: 626-640.
Budovich, LS 2021, Effects of heavy metals in soil and plants on ecosystems and the economy. Caspian Journal of Environmental Sciences, 19: 991-997.
Bushuty, D & Shanshan, N 2020, The effect of moringa leaves powder on hypercholesterolemic male rats and the possibility of adding to some vegetable recipes. Journal of Research in the Fields of Specific Education, 6: 635- 659.
Cajuday, L & Pocsidio, G 2010, Effects of Moringa oleifera lam. (Moringaceae) on the reproduction of male mice (mus musculus). Journal of Medicinal Plants Research, 4: 1115-1121.
Chandra, AK, Chatterjee, A, Ghosh, R & Sarkar, M 2007, Effect of curcumin on chromium-induced oxidative damage in male reproductive system. Environmental Toxicology and Pharmacology Journal, 24: 160-166.
Cho, A, Jeon, S, Kim, M, Yeo, J, Seo, K, Choi, M & Lee, M 2010, Chlorogenic acid exhibits anti-obesity property and improves lipid metabolism in high-fat diet-induced-obese mice. Food and Chemical Toxicology, 48: 937-943.
Coppin, J, Xu, Y, Chen, H, Pan, M, Ho, C, Juliani, R et al. 2013, Determination of flavonoids by LC/MS and anti-inflammatory activity in Moringa oleifera. Journal of Functional Foods, 5: 1892-1899.
Das, N, Ganguli, D & Dey, S 2015, Moringa oleifera Lam. seed extract prevents fat diet induced oxidative stress in mice and protects liver cell-nuclei from hydroxyl radical mediated damage. Indian Journal of Experimental Biology, 53: 794-802.
Diemer, T, Allen, J, Hales, K & Hales, D 2003, Reactive oxygen disrupts mitochondria in MA-10 tumor Leydig cells and inhibits steroidogenic acute regulatory (StAR) protein and steroidogenesis. Endocrinology, 144: 2882-2891.
Doisy, R, Streeten, D, Freiberg, J & Schneider, A 2013, Chromium metabolism in man and biochemical effects. Trace Elements in Human Health and Disease, 2: 79-104.
Drury, RAB, Wallgton, EA & Cameron, SR 1985, Carleton's histological techniques. 4th ed. Oxford University Press, New York, 343 p.
Fallah, A, Mohammad Hasani, A & Colagar, A 2018, Zinc is an essential element for male fertility: A review of Zn roles in men's health, germination, sperm quality, and fertilization. Journal of Reproduction & Infertility, 19: 69-81.
Fathima, K & Priyanka, S 2017, Ameliorative effect of Emblica officinalis in potassium dichromate induced toxicity in rats. European Journal of Pharmaceutical and Medical Research, 4: 267-274.
Folch, J, Less, M & Stanley, GH 1957, A simple method for the isolation and purification of total lipids from animal tissue. Journal of Biological Chemistry, 266: 497-509.
Fu, S, Liu, J, Lee, K, Tang, F, Fang, K, Yang, C, Su, C, Chen, H, Hsu, R & Chen, Y 2020, Cr (VI) induces ROS-mediated mitochondrial-dependent apoptosis in neuronal cells via the activation of Akt/ERK/AMPK signalling pathway. Toxicology in Vitro, 65: 1-10.
Fuhrman, B & Aviram, M 2001, Flavonoids protect LDL from oxidation and attenuate atherosclerosis. Current Opinion in Lipidology, 12: 41-48.
Ganatra, T, Umang, H, Payal, N, Tusharbindu, R & Pravin, R 2012, A panoramic view on pharmacognostic, pharmacological, nutritional, therapeutic and prophylactic values of Moringa oleifera. International Research Journal of Pharmacy, 3: 1-7.
Ghasi, S, Nwobodo, E & Ofili, J 2000, Hypocholesterolemic effects of crude extract of leaf of Moringa oleifera Lam in high-fat diet fed Wister rats. Journal of Ethnopharmacology, 69: 21- 25.
Gilbert, H, Stump, D & Roth, F 1984, A method to correct for errors caused by generation of interfering compounds during erythrocyte lipid peroxidation. Analytical Biochemistry, 137: 282-286.
Goldfrank, L, Lewin, N, Flomenbaum, N & Howland, M 1982, The pernicious panacea: herbal medicine. Hospital Physician, 18: 64.
Gopalakrishnan, L, Devarai, K, Kumara, S et al. 2016, Moringa oleifera: A review on nutritive importance and its medicinal application. Food Science and Human Wellness, 5: 49-56.
Gupta, S, Singh, S & Sunita, S 2015, Tolerance against heavy metal toxicity in cyanobacteria: role of antioxidant defence system. International Journal of Health Sciences and Pharmacy, 7: 9-16.
Ibrahim, W, Oda, S & Khafaga, A 2017, Pathological evaluation of the effect of zinc oxide nanoparticles on chromium-induced reproductive toxicity in male albino rats. Alexandria Journal of Veterinary Sciences, 53: 24-32.
Illingworth, P, Groome, N, Byrd, W et al. 1996, Inhibin-B: A likely candidate for the physiologically important form of inhibin in men. The Journal of Clinical Endocrinology & Metabolism, 81: 1321-1325.
Janbakhsh, S, Hosseini Shekarabi, SP, Shamsaie Mergan, M 2018, Nutritional value and heavy metal content of fishmeal from the Southwest Caspian Sea.  Caspian Journal of Environmental Sciences, 16: 307-317
Khalil, W, Ismail, R & El Ratel, I 2019, Efficacy of dietary Moringa oleifera leaves supplementation on productivity, carcass traits, hemato-biochemical parameters, antioxidants status and immune response in heat stressed growing rabbits. Egyptian Journal of Nutrition and Feeds, 22: 521-534.
Kortenkamp, A 2011, Are cadmium and other heavy metal compounds acting as endocrine disrupters? Metal Ions in Life Sciences, 8: 305-317.
Kusev, P, Purser, H, Heilman, R, Cooke, A, Van Schaik, P et al. 2017, Understanding risky behaviour: the influence of cognitive, emotional and hormonal factors on decision- making under risk. Frontiers in Psychology, 8: 102.
León, L, Otero, W & Gómez, M 2015, Fever, jaundice and hepatitis: it is not always a viral infection. Revista colombiana de Gastroenterología, 30: 287-291.
Lopes, J, Araujo, S, Estevam, C, Lima, C, Carvalho, C, Lima, F & Marcal, A 2017, Molecular mechanisms of muscle glucose uptake in response to resistance exercise: a review. Journal of Exercise Physiology online, 20: 200-211.
Lu, SC 1999, Regulation of hepatic glutathione synthesis: Current concepts and controversies. Federation of American Societies for Experimental Biology Journal, 13: 1169-1183.
Luqman, S, Srivastava, S, Kumar, R, Maurya, A & Chanda, A 2012, Experimental assessment of moringa oleifera leaf and fruit for its anti-stress, antioxidant, and scavenging potential using in vitro and in vivo assays. Evidence-based Complementary and Alternative Medicine, Article ID 519084, 12 p.
Mac Sween, RMN & Whaley, K 1992, Liver, biliary tract and pancreas. In: RMN, Mac Sween & K Whaley (eds.). Muir’s Text book of pathology, 13th Edition, Thomson Press (India) Ltd., New Delhi, 741-803.
Meachem, S, Nieschlag, E & Simoni, M 2001, Inhibin B in male reproduction: pathophysiology and clinical relevance. European Journal of Endocrinology, 145: 561-571.
Mbikay, M 2012, Therapeutic potential of Moringa oleifera leaves in chronic hyperglycemia and dyslipidemia: A review. Frontiers in Pharmacology, 3: 24.
Mehdinia, SM, Rastgoo, TPB, Abdul Latif Moeinian, K 2017, Effects of pH, particle size and porosity of raw rice husk and its silica on removing lead and hexavalent chromium from aqueous solution. Caspian Journal of Environmental Sciences, 15: 263-270.
Mohamed, M 2019, Molecular effects of Moringa leaf extract on insulin resistance and reproductive function in hyperinsulinemic male rats. Journal of Diabetes and Metabolic Disorders, 18: 487-494.
Mohamed, SS & Fayed, A 2020, Anti-obesity synergistic effect of pomegranate seed oil (PSO) and Arabic gum (AG) in albino rats. International Journal of Veterinary Science, 9: 84- 89.
Momo, Ch, Ferdinand, N, Bebe, N et al. 2019, Oxidative effects of potassium dichromate on biochemical, hematological characteristics, and hormonal levels in rabbit doe (Oryctolagus cuniculus). Veterinary Sciences, 6: 1-12.
Moron, M, Depierre, J & Mennervik, B 1979, Levels of glutathione, glutathione reductase and glutathione-S-transferase activities in rates lung and liver. Biochimica et Biophysica Acta, 582: 67-78.
Mossa, A, Heikal, T, Belaiba, M, Raoelison, E, Ferhout, H & Bouajila, J 2015, Antioxidant activity and hepato-protective potential of Cedrelopsis grevei on cypermethrin induced oxidative stress and liver damage in male mice. Complementary and Alternative Medicine, 15: 1-10.
Nayak, G, Honguntikar, S, Kalthur, S, D’Souza, A et al. 2016, Ethanolic extract of moringa oleifera lam. leaves protect the pre-pubertal spermatogonial cells from cyclophosphamide-induced damage. Journal of Ethnopharmacology, 182: 101-109.
Nayak, G, Rao, A, Mullick, P, Mutalik, S, Kalthur, S, Kumar Adiga, S & Kalthur, G 2020, Ethanolic extract of moringa oleifera leaves alleviate cyclophosphamide-induced testicular toxicity by improving endocrine function and modulating cell specific gene expression in mouse testis. Journal of Ethnopharmacology, 259:112922.
Nudler, S, Quinteros, F, Miler, E, Cabilla, J, Ronchetti, S & Duvilanski, B 2009, Chromium VI administration induces oxidative stress in hypothalamus and anterior pituitary gland from male rats. Toxicology Letters, 185: 187-190.
O’Brien, T, Xu, J & Patierno, S 2001, Effects of glutathione on chromium-induced DNA crosslinking and DNA polymerase arrest. Molecular and Cellular Biochemistry, 222: 173-182.
Olayaki, L, Irekpita, J, Yakubu, M & Ojo, O 2015, Methanolic extract of moringa oleifera leaves improves glucose tolerance, glycogen synthesis and lipid metabolism in alloxan-induced diabetic rats. Journal of Basic and Clinical Physiology and Pharmacology, 26: 585-593.
Ong, K, Hsu, A & Tan, B 2013, Anti-diabetic and anti-lipidemic effects of chlorogenic acid are mediated by AMPK activation. Biochemical Pharmacology, 85: 1341-1351.
Oseni, OA & Idowu, AS 2014, Inhibitory activity of aqueous extracts of horseradish Moringa oleifera (lam) and nutmeg Myristica fragrans (houtt) on oxidative stress in Alloxan induced diabetic male Wistar albino rats. American Journal of Biochemistry and Molecular Biology, 4: 64-75
Rao, AV & Shaha, C 2001, Multiple glutathione S-transferase isoforms are present on male germ cell plasma membrane. FEBS Letters, 507: 174-180.
Reddy, V, Urooj, A, Sairam, S, Ahmed, F & Prasad, N 2017, Hypocholesterolemic effect of Moringa oleifera polyphenols in rats fed high fat-cholesterol diet. Malaysian Journal of Nutrition, 23: 473- 478.
Padashetty, S & Mishra, S 2007, Aphrodisiac studies of Tricholepis glaberrima. with supportive action from antioxidant enzymes. Pharmaceutical Biology, 45: 580-586.
Pechova, A & Pavlata, L 2007, Chromium as an essential nutrient: A review. Veterinarni Medicina, 52: 1-18.
Pineau, C, Sharpe, R, Saunders, P, Gerard, N & Jegou, B 1990, Regulation of Sertoli cell inhibin production and inhibin a-subunit mRNA levels by specific germ cell types. Molecular and Cellular Endocrinology, 72: 12-22.
Rao, A & Shaha, C 2000, Role of glutathione S-transferases in oxidative stress-induced male germ cell apoptosis. Free Radical Biology & Medicine, 29: 1015-1027.
Reitman, S & Frankel, S 1957, Colorimetric method for the determination of serum transaminases. American Journal of Clinical Pathology, 28: 56-61.
Sadek, KM 2014, Chemotherapeutic efficacy of an ethanoic Moringa oleifera leaf extract against chromium-induced testicular toxicity in rats. Andrologia, 46: 1047-1054.
Saalu, L, Osinubi, A, Akinbami, A, Yama, O, Oyewopo, A &  Enaibe, B 2011, Moringa oleifera lamarck (drumstick) leaf extract modulates the evidences of hydroxyurea –induced testicular derangement. International Journal of Applied Research in Natural Products, 4: 32-45.
Saha, J, Choudhuri, S & Choudhuri, D 2017, Effect of sub-chronic exposure to chromium on hematological and biochemical parameters of male albino rat. Asian Journal of Pharmaceutical and Clinical Research, 10: 345-348.
Saleh Ibrahim, A, Chyad Al-Hamadani, RF, Fahim Chyad, T, H. Ali, S 2022, Using ozone for activation of manufactured porous media to improve the removal efficiency of heavy metals from industrial wastewater. Caspian Journal of Environmental Sciences, 20: 283-294.
SAS Institute 2004, SAS User’s Guide: Statistics. Cary (NC): SAS Institute Inc.
Sharifudin, S, Fakurazi, S, Hidayat, M, Hairuszah, I et al. 2012, Therapeutic potential of Moringa oleifera extracts against acetaminophen-induced hepatotoxicity in rats. Pharmaceutical Biology, 51: 279-288.
Shi, H, Dong, L, Dang, X, Liu, Y, Jiang, J, Wang, Y, Lu, X & Guo, X 2013, Effect of chlorogenic acid on LPS-induced pro-inflammatory signalling in hepatic stellate cells. Inflammation Research, 62: 581-587.
Siddhuraju, P & Becker, K 2003, Antioxidant properties of various solvent extracts of total phenolic constituents from three different agroclimatic origins of drumstick tree (Moringa oleifera Lam.) leaves. Journal of Agricultural and Food Chemistry, 51: 2144-2155.
Singh, A, Rana, H, Tshabalala, T, Kumar, R, Gupta, A, Ndhlala, A & Pandey, A 2019, Phytochemical, nutraceutical and pharmacological attributes of a functional crop Moringa oleifera Lam: An overview. South African Journal of Botany, 129: 209-220.
Singh, J, O’Neill, C & Handelsman, D 1995, Induction of spermatogenesis by androgens in gonadotropin-deficient (HPG) mice. Endocrinology, 136: 5311-5321.
Sobhanardakani, S 2019, Heavy metals health risk assessment through consumption of some foodstuffs marketed in city of Hamedan, Iran. Caspian Journal of Environmental Sciences, 17: 175-183.
Soudani, N, Bouaziz, H, Sefi, M, Chtourou, Y, Boudawara, T & Zeghal, N 2013, Toxic effects of chromium (VI) by maternal ingestion on liver function of female rats and their suckling pups. Environmental Toxicology, 28: 11-20.
Srivastava, M, Dhakad, PK & Srivastava, B 2020, A review on medicinal constituents and therapeutic potential of Moringa oleifera. Universal Journal of Plant Science, 8: 22-33.
Stohs, S & Bagchi, D 1995, Oxidative mechanisms in the toxicity of metal-ions. Radiology-Free Medical Journals, 18: 321-336.
Trapani, L, Segatto, M & Pallottini, V 2012, Regulation and deregulation of cholesterol homeostasis: The liver as a metabolic “power station”. World Journal of Hepatology, 4: 184- 190.
Trigo, C, Castelló, M, Ortolá, M, García Mares, F & Soriano, M 2021, Moringa oleifera: an unknown crop in developed countries with great potential for industry and adapted to climate change. Foods, 10: 1- 14.
Vaknin, Y & Mishal, A 2017, The potential of the tropical “miracle tree” Moringa oleifera and its desert relative Moringa peregrina as edible seed-oil and protein crops under Mediterranean conditions. Scientia Horticulturae, 225: 431-437.
Vinodini, N, Chatterjee, P, Amemarsoofi, A, Suman, V & Pai, S 2014, Evaluation of liver functions with moringa oleifera leaf extract in cadmium induced adult Wistar albino rats. International Journal of Plant, Animal and Environmental Sciences, 4: 104-106.
Wang, X, Lou, X, Shen, Y, Xing, M & Xu, L 2010, Apoptosis-related protein changes induced hexavalent chromium in mice liver. Environmental Toxicology, 25:77-82.
Waterman, C, Rojas Silva, P, Tumer, T et al. 2015, Isothiocyanate-rich Moringa oleifera extract reduces weight gain, insulin resistance, and hepatic gluconeogenesis in mice. Molecular Nutrition and Food Research 59: 1013- 1024.
Weinbauer, G, Barlett, J, Fingscheid, U, Tsonis, C, de Kretser, D & Nieschlag, E 1989, Evidence for a major role of inhibin in the feedback control of FSH in the male rat. Journal of Reproduction & Infertility, 85: 355-362.
Yam-Canul, P, Chirino, Y, Sanchez-Gonzalez, D, Martinez Martinez, C, Cruz, C, Villanueva, C & Pedraza- Chaverri, J 2008, Nordihydroguaiaretic acid attenuates potassium dichromate induced oxidative stress and nephrotoxicity. Food and Chemical Toxicology, 46: 1089-1096.
    Yousif, AS & Ahmed, AA 2009, Effects of cadmium (Cd) and lead (Pb) on the structure and function of thyroid gland.  African Journal of Environmental Science and Technology, 3: 78-85.
Zhang, Y, Ma, Y, Liang, N, Liang, Y, Lu, C & Xiao, F 2019, Blockage of ROS-ERK-DLP1 signalling and mitochondrial fission alleviates Cr (VI)-induced mitochondrial dysfunction in.